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Keywords:

  • bufonidae;
  • competition;
  • invasive species;
  • larvae;
  • Rhinella marina

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1. Native to the Americas, cane toads Bufo marinus are an invasive species causing substantial ecological impacts in Australia. We need ways to control invasive species such as cane toads without collateral damage to native fauna.

2. We explored the feasibility of suppressing survival and growth of cane toad tadpoles via competition with the tadpoles of native frogs. Compared to the invasive toads, many native frogs breed earlier in the season and their tadpoles grow larger and have longer larval periods. Hence, adding spawn or tadpoles of native frogs to toad-breeding sites might increase tadpole competition, and thereby reduce toad recruitment.

3. Our laboratory trials using tadpoles of eight native frog species gave significant results: the presence of six of these species (Cyclorana australis, C. longipes, Litoria caerulea, L. dahlii, L. rothii and L. splendida) reduced toad tadpole survival and/or size at metamorphosis. Litoria caerulea also increased the duration of the larval period of cane toad tadpoles. Tadpoles of the other two frog species (Litoria rubella and Litoria tornieri) did not affect survival or growth of larval cane toads any more than did an equivalent number of additional toad tadpoles. Native frog species with larger tadpoles exerted greater negative effects on toad tadpoles than did native species with smaller tadpoles.

4.Synthesis and applications. Encouraging the general public to construct and restore waterbodies in peri-urban areas to build up populations of native frogs – especially the much-loved green tree frog Litoria caerulea– could help to reduce recruitment rates of invasive cane toads in Australia.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Invasive species pose a substantial threat to ecosystems in most parts of the world, but controlling the invaders is difficult. In many situations, physical removal is ineffective due to factors such as high reproductive rates of the invasive species (Blossey, Skinner & Taylor 2001; Wheeler, Pemberton & Raz 2007). Biological control thus offers the only possible solution in such cases, but the history of biocontrol attempts is littered with case-histories of failure (e.g. Thrall & Burdon 2004; Boughton & Pemberton 2008; van Klinken & Flack 2008). Indeed, such control attempts often have backfired, with the ‘solution’ to an invasive-species problem ultimately proving worse than the problem it was brought in to ameliorate. This is the case for cane toads in Australia, imported in 1935 to control agricultural pests in commercial sugarcane plantations (Lever 2001). Similarly, mongoose were introduced to many areas worldwide to reduce the numbers of snakes, and hence the risk of snakebite to humans (Hays & Conant 2007).

Thus, we urgently need novel approaches to invasive-species control, that do not involve the potential problems that may arise if other non-indigenous taxa (e.g. predators, parasites, competitors or pathogens) are brought in to attack the identified pest species (Simberloff & Stiling 1996a,b). In the present paper, we explore one such approach: to encourage components of the native fauna that have negative effects on the invader. Previous studies have shown that this approach has the potential to assist in the control of invasive flora and fauna (Klug et al. 2008; Perry, Cronin & Paschke 2009; Prober & Lunt 2009; Santos et al. 2009; Ward-Fear, Brown & Shine 2010).

Cane toads Bufo marinus Linnaeus, 1758 (see Pramuk et al. 2008 for suggested nomenclatural change to Rhinella marina) are large, highly toxic anurans native to the Americas but translocated to many countries for the purpose of controlling insects (Lever 2001). Introduced to northeastern Australia in 1935, the toads have since spread over more than a million square kilometres, and caused widespread mortality of native predators (e.g. snakes, lizards, crocodiles, marsupials) that attempt to consume these highly toxic invaders (Covacevich & Archer 1975; Lever 2001; Phillips, Brown & Shine 2003; Letnic, Webb & Shine 2008). Cane toads deposit large numbers of small eggs (to at least 30,000 eggs per clutch) mainly in shallow pools with open (unvegetated) gradually sloping muddy banks (Hagman & Shine 2006). Where toads co-occur with native frogs, such waterbodies often are used as spawning sites by both types of anurans (Crossland et al. 2008). Previous experimental studies have revealed strong exploitation and/or interference competitive interactions among tadpoles of different species under such circumstances (Alford 1999), including between cane toad tadpoles and the larvae of Australian frog species (Alford 1999; Williamson 1999; Crossland, Alford & Shine 2009).

The primary focus of previous work has been on the ecological impact of cane toads, particularly the degree to which the invasion of toads has reduced recruitment of native species. In the present work we focus on the other side of the coin: the idea that tadpoles of native frog species may suppress recruitment of cane toads, via competitive interactions during larval life (see also Crossland, Alford & Shine 2009). In many parts of Australia, populations of native frogs have been decimated by anthropogenic disturbances, including water pollution and pond-side habitat degradation. Thus, the invasive toads (which actively select disturbed sites for breeding: Hagman & Shine 2006; Semeniuk, Lemckert & Shine 2007) might have flourished partly because of a lack of competitors that would otherwise have been present. If the effects of native frogs on cane toads are strong, we might be able to use them as a component of cane toad control. Thus, we assessed the negative effects of the tadpoles of eight species of native frogs on survival of cane toad larvae, rates of growth (size and mass of metamorphs) and development (time to metamorphosis).

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Study species and area

We studied interactions between invasive cane toads and native frogs on the Adelaide River floodplain, 60 km east of Darwin in the Australian wet-dry tropics. Our experiments used seven common hylid species in this area: Cyclorana australis Gray, 1842 (giant frog), C. longipes Tyler & Martin, 1977 (long-footed frog), Litoria caerulea White, 1790 (green tree frog), L. dahlii Boulenger, 1896 (Dahl’s aquatic frog), L. rothii De Vis, 1884 (Roth’s tree frog), L. rubella Gray, 1842 (red tree frog) and L. tornieri Nieden, 1923 (Tornier’s frog) whose tadpoles occur in a wide range of waterbodies in this area, over an extended period of the year (December to February: M. Crossland, unpublished data). We also tested Litoria splendida Tyler, Davies & Martin, 1977 (magnificent tree frog); although not native to our study area, this species occurs in other areas of the Northern Territory and Western Australia that will soon be colonized by cane toads. Tadpoles of all species tested have a long larval phase (>1 month) under natural conditions (Tyler, Crook & Davies 1983; M. Crossland, personal observation). We have recorded frequent co-occurrence of breeding activity of the first seven species with Bufo marinus at our study site (Table 1); because these native tadpoles are susceptible to cane toad toxins, their overlap with toad breeding means that frog tadpoles are killed in the field when they ingest newly laid toad eggs (over 4 months, we recorded fatal poisoning of >1300 tadpoles of 10 species at our study site: Crossland et al. 2008). However, frog tadpoles usually do not attempt to consume live toad tadpoles, and so most are at risk only briefly, immediately following toad-spawning (Crossland & Alford 1998; Crossland & Shine 2010).

Table 1.   Observations of co-occurrence of breeding activity of cane toads with seven of the eight native frog species used in the current study
PondCyclorana australisCyclorana longipesLitoria caeruleaLitoria dahliiLitoria rothiiLitoria rubellaLitoria tornieri
  1. These data were collected at 15 ponds in the Middle Point area (Adelaide River floodplain, Northern Territory). The Table shows the number of occasions where we recorded co-occurrence of cane toad breeding (as evidenced by calling activity, eggs, tadpoles or metamorphs) with breeding by native frogs (based on the same criteria). Observations were made during the wet seasons of 2006–2007 to 2008–2009.

 153 286 
 2    836
 3   11  
 4    1 1
 576 361 
 6    11 
 7    1  
 856 1542
 9  4 11 
10  3 11 
111 2 313
121   3  
13    1  
1431 233 
15    43 

Effects of frog tadpoles on survival and growth of toad tadpoles

Due to variation in species availability, we tested the effects of native tadpoles on cane toad tadpoles in two experiments. Tadpoles of C. australis, C. longipes, L. caerulea, L. dahlii, L. rothii, L. rubella and L. tornieri were derived from eggs collected in natural ephemeral ponds that are also used by cane toads as breeding sites during the wet season (M. Crossland, personal observation). At the time of collection, cane toad tadpoles were not present in the ponds. Tadpoles of L. splendida were obtained from adult frogs that bred naturally in captivity. Cane toad tadpoles were obtained by injecting local field-collected adults with 0·25 mg mL−1 of leuprorelin acetate (Lucrin, Abbott Australia), to induce amplexus and spawning. Prior to experiments, all tadpoles were maintained in 750 L mesocosms containing 600 L of non-chlorinated bore water. Tadpoles were fed algae pellets and frozen lettuce, and water was changed twice weekly. The tadpoles used in the experiments were haphazardly selected from holding tanks and added to experimental bins as described below.

Experiments were run using plastic bins (60 × 40 × 40 cm), each filled with 65 L water and located in a covered building exposed to ambient temperatures. At the start of each experiment, we added a 2-cm layer of substrate taken from two nearby dry ephemeral ponds (used by toads and frogs as breeding sites) and 3 g of crushed vegetable food to each bin (Experiment 1: HBH Pet Products vegetable wafer pellets – crude protein 33%, crude fat 6%, crude fibre 5%, moisture 10%; Experiment 2: HBH Pet Products algae grazer pellets – crude protein 28%, crude fat 6%, crude fibre 6%, moisture 10%). We did not change the water, nor provide additional food, for the remainder of the experiment.

Each experiment was a randomized block design with treatments consisting of 10 B. marinus, 20 B. marinus, or 10 B. marinus plus 10 tadpoles per native species (i.e. apart from the control treatment [10 toad tadpoles only], each enclosure contained 10 toad tadpoles plus 10 other tadpoles [either toads or one of the frog taxa]; N = 5 replicates per treatment). Experiment 1 tested C. australis and L. dahlii (i.e. 4 treatments total: 10 Bufo, 20 Bufo, 10 Bufo plus 10 C. australis; 10 Bufo plus 10 L. dahlii); all B. marinus tadpoles came from the same clutch. Experiment 2 used toad tadpoles from an additional two Bufo clutches (mixed) and tested the remaining six native species (i.e. 8 treatments total: 2 Bufo treatments and 6 ‘Bufo plus native frog’ treatments).

At the start of each experiment, we randomly selected 10 tadpoles per species and recorded snout-vent length (SVL; with digital callipers), mass (Scout Pro Balance, OHAUS) and developmental stage (Gosner 1960). Mass was measured after tadpoles were blotted dry with absorbent paper. For all species, native tadpoles were older, and hence larger and at a more advanced developmental stage, than toad tadpoles (Table 2). We checked experimental bins daily and removed dead individuals and individuals close to metamorphosis (i.e. those with both forelimbs present). Metamorphosing animals were kept in 1 L rectangular plastic containers with a little water until tail resorption was complete, at which point we recorded time to metamorphosis, snout-urostyle length (SUL) and mass (blotted dry weight).

Table 2.   Body sizes (mean and range) and Gosner stages for tadpoles as measured at the beginning of the experiments
 Body size (mm)Mass (g)Gosner stage
  1. Bufo marinus 1 = individuals used in Experiment 1, Bufo marinus 2 = individuals used in Experiment 2.

Bufo marinus 16·41 (6·10–7·20)0·04 (0·01–0·04)25 (25)
Bufo marinus 25·58 (5·07–6·61)0·03 (0·01–0·05)27·18 (26–28)
Cyclorana australis21·58 (18·80–24·90)1·27 (0·77–1·35)31 (28–33)
Cyclorana longipes13·30 (11·22–16·59)0·38 (0·22–0·57)27·7 (26–29)
Litoria caerulea13·82 (12·50–15·50)0·40 (0·30–0·54)31·2 (29–34)
Litoria dahlii18·89 (16·02–21·36)0·78 (0·49–0·82)31·3 (28–34)
Litoria rothii13·27 (12·19–15·03)0·35 (0·24–0·46)28 (27–31)
Litoria rubella9·33 (6·57–11·09)0·14 (0·08–0·20)30·1 (27–33)
Litoria splendida12·43 (10·39–13·87)0·30 (0·20–0·37)30 (27–33)
Litoria tornieri9·27 (8·14–10·77)0·14 (0·12–0·20)27·6 (27–28)

We terminated the experiments after 85 days (Experiment 1) and 70 days (Experiment 2). At this time, the few remaining B. marinus tadpoles (<5% remaining in both experiments; all in treatments exposed to native frog tadpoles) were still in mid-developmental stages (stages 30–34). Thus, our data represent outcomes for ≥95% of toad tadpoles that were added to experimental bins at the start of the experiments.

Statistical analyses

We combined the data for both experiments using ‘experiment’ as a random effect, and compared body sizes at metamorphosis (length and mass), durations of larval life and proportion of survivors to metamorphosis among treatments using anovas. Analyses for body size and larval period were based on mean values per experimental container. Following significant anova, post hoc Tukey’s HSD tests were performed to determine the location of significant variation. Proportional survival data were arcsine-square root transformed prior to analysis.

To assess whether tadpole body sizes affect the intensity of suppression of cane toad larvae, we initially ran a principal component analysis (PCA) to reduce the cane toad variables (proportion survival, larval period, SVL and mass) to a single principal component (PC1) and examined the relationship of each response variable with PC1. We then regressed PC1 against the SVL of the competitor tadpoles at the start of the experiment using linear regression. Analyses were performed using jmp 5·0·1 software (SAS 2002).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Effects of frog tadpoles on survival and growth of toad tadpoles

All four variables that we measured were significantly affected by experimental treatment (body length –F9,42 = 64·55, P < 0·0001; body mass –F9,42 = 53·34, P < 0·0001; survival –F9,49 = 16·41, P < 0·0001; duration of larval period F9,42 = 2·48, P = 0·023). Post hoc (Tukey) tests showed that the presence of several species of native tadpoles reduced mean survival of cane toad tadpoles (magnitude of reduction in toad survival: C. australis 70%, C. longipes 67%, L. caerulea 83%, L. rothii 78%, L. splendida 81%), metamorphic body length (magnitude of reduction in SUL: C. australis 20%, C. longipes 15%, L. caerulea 10%, L. dahlii 12%, L. splendida 16%) and metamorphic body mass (C. australis 57%, C. longipes 30%, L. caerulea 30%, L. dahlii 47%, L. splendida 37%) significantly more than did addition of the same number of conspecific toad tadpoles (P < 0·05; Fig. 1). In contrast, the effects of L. rubella and L. tornieri tadpoles on survival rate and metamorphic body length and mass of cane toads were equivalent to those of the same number of conspecific toad tadpoles (P > 0·05; Fig. 1). Addition of L. caerulea tadpoles also increased the mean larval period of cane toads (by 61%), significantly more than did addition of the same number of conspecific toad tadpoles (P < 0·05; Fig. 1). Frog tadpoles of the other species affected the duration of larval periods of cane toads to a similar degree as did the same number of conspecific toad tadpoles (P > 0·05; Fig. 1).

image

Figure 1.  Effects of larval densities and presence of heterospecific larvae on (a) survival of cane toad Bufo marinus tadpoles, (b) the duration of the larval period, and (c, d) their body sizes at metamorphosis. The experimental treatments were (left to right): (1) 10 B. marinus tadpoles, (2) 20 B. marinus tadpoles, (3) 10 B. marinus tadpoles plus 10 Cyclorana australis tadpoles, (4) 10 B. marinus tadpoles plus 10 Cyclorana longipes tadpoles, (5) 10 B. marinus tadpoles plus 10 Litoria caerulea tadpoles, (6) 10 B. marinus tadpoles plus 10 Litoria dahlii tadpoles, (7) 10 B. marinus tadpoles plus 10 Litoria rothii tadpoles, (8) 10 B. marinus tadpoles plus 10 L. rubella tadpoles, (9) 10 B. marinus tadpoles plus 10 L. splendida tadpoles, and (10) 10 B. marinus tadpoles plus 10 L. tornieri tadpoles. The Figure shows mean values plus associated standard errors.

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Based on the combined data set, the size of competitor tadpoles at the start of the experiments was negatively associated with PC1 values (R2 = 0·419, F = 5·78, P = 0·042; Fig. 2). That is, the negative effects of competitor tadpoles on cane toad tadpoles (low survival, increased larval period, and reduced size at metamorphosis) increased as the size of the competitor tadpole increased. Relative to their body size, tadpoles of L. caerulea, L. splendida, C. australis, and C. longipes had the greatest negative effect on cane toad tadpoles (Fig. 2).

image

Figure 2.  Relationship between competitor tadpole body size (SVL) and the first principal component of cane toad responses (high ‘toad viability scores’ indicate larger toad metamorph size, higher survival, and briefer larval duration). Species names are shown next to each point. In each case the PC axis is based on mean responses of five replicates of 10 cane toad tadpoles that were exposed to 10 tadpoles of the indicated species.

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Although our study was designed to evaluate the effects of frog tadpoles on toad tadpoles rather than vice versa, data on frog survival and metamorphic rates are relevant because frog species with high survival may be able to suppress toad tadpoles for longer time periods. Survival and metamorphic rates were high for all species except L. rothii and L. tornieri (Table 3). Litoria rothii was the only species to experience significant mortality early in the experiment (19 of 50 tadpoles died within the first 5 days, due to attempted predation on toxic toad tadpoles). In contrast, with the exception of one individual, tadpoles of L. tornieri did not begin to experience mortality until after day 25.

Table 3.   Number of tadpoles and metamorphs of native frogs surviving to various times through the experiments (from an initial cohort of 50)
SpeciesNumber of tadpoles on Day 5Number of tadpoles on Day 25Number of tadpoles on Final DayNumber of metamorphs TotalTotal number of survivors (tadpoles plus metamorphs)
  1. The duration of study was 85 days for Experiment 1 and 70 days for Experiment 2 (see text for details).

C. australis504429736
C. longipes504835237
L. caerulea49624244
L. dahlii504292736
L. rothii312920020
L. rubella5027132437
L. splendida5015103444
L. tornieri504910010

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

In our laboratory trials, the presence of native tadpoles strongly affected cane toad tadpoles in ways likely to reduce organismal fitness. The link to fitness is unambiguous for survival rate (individuals that die as tadpoles can never reproduce), which was affected far more by the presence of native tadpoles of five species (C. australis, C. longipes, L. caerulea, L. rothii and L. splendida) than by addition of the same number of conspecific (toad) tadpoles. Body size of toads at metamorphosis also may be linked to fitness because in anurans, larger size at metamorphosis often correlates with higher post-metamorphic survival rates (Berven & Gill 1983), earlier age of maturity (Smith 1987) and larger size at first reproduction (Berven & Gill 1983). Such body-size differences can influence adult anuran reproductive fitness because female clutch size (Clarke 1974; Howard 1978a) and male mating success (Howard 1978a,b; Wilbur, Rubenstein & Fairchild 1978; Ryan 1980; Berven 1981) increase with body size in at least some species. For cane toads specifically, studies have shown that smaller metamorphs may be less likely to survive if exposed to predators, parasites or a desiccating environment (see below). Both body length and body mass of toad metamorphs were reduced (compared to the case with a similar total density of toad tadpoles alone) if the toad tadpoles were raised with C. australis, L. dahlii, L. caerulea, L. splendida or C. longipes. The effects of tadpoles of the other three species of native frogs (L. rothii, L. rubella and L. tornieri) on toad metamorph size were similar in magnitude to the effects of the same number of toad tadpoles. The fitness effects of changes to the duration of larval life are more complex to evaluate, but in many ephemeral waterbodies a prolongation of development is likely to result in higher mortality rates due to increased exposure to aquatic predators and increased probability of waterbodies drying out before the young anurans metamorphose (Lane & Mahony 2002; Loman 2002). In our experiments, the strongest effect on extending toad larval duration came from the addition of L. caerulea (Fig. 1).

Competition appears to be solely responsible for these effects except for the case of Litoria rothii, the only species whose tadpoles attacked live toad tadpoles and attempted to consume them. This predation (which we noticed within the first 5 days of the experiment) explains the low survival of toad tadpoles in the treatment with L. rothii (Fig. 1). Litoria rothii tadpoles in this treatment also experienced high mortality (Table 3), because of the toads’ toxic effects following ingestion (see Hayes et al. 2009). This reduced density of L. rothii may have minimised negative competitive effects on growth and development of toad tadpoles. The only other native species to experience high mortality was L. tornieri. In this case, however, mortality occurred much later in the experiment (Table 3): by day 25 only 1 of 50 L. tornieri tadpoles had died, but 36 of 50 (72%) toad tadpoles in this treatment had metamorphosed. Thus, the minimal effects of L. tornieri on toad tadpole performance were not due to low survivorship of L. tornieri tadpoles.

In combination with earlier reports (viability and growth of cane toad larvae are reduced by the presence of frog tadpoles, Opisthodon ornatus: Alford 1999; Crossland, Alford & Shine 2009), our results suggest that the larvae of cane toads are affected by competition with larvae from many species of native Australian frogs. Nevertheless, some native species have relatively little competitive effect on cane toad tadpoles (e.g. Limnodynastes tasmaniensis, L. terraereginae and Notaden bennetti: Williamson 1999). Whether this variation also reflects aspects of experimental design (e.g. the size class of native tadpoles used: Steinwascher 1978; Werner & Anholt 1996) is unclear. In our trials, the size disparity between toad tadpoles and frog tadpoles was a major determinant of competitive suppression (Table 2; Fig. 2), perhaps reflecting higher rates of consumption of resources and production of waste products by larger animals (e.g. Richter-Boix, Llorente & Montori 2007). The effects of the presence of the smallest native tadpoles used in our study (L. tornieri and L. rubella) were similar to those caused by the addition of similar numbers of cane toad tadpoles.

The mechanism of suppression induced by frog tadpoles (and other toad tadpoles) warrants further study. The simplest possibility is direct competition for food, but the negative effects on toad tadpoles also might be mediated by behavioural interactions, or by chemical or biological substances. In some larval anurans, competitive suppression is mediated by the protist Prototheca richardsi (Beebee 1991; Griffiths, Edgar & Wong 1991; Griffiths, Denton & Wong 1993; see Baker, Beebee & Ragan 1999 for taxonomic revision to Anurofeca richardsi) rather than direct rivalry for food or other resources (summary in Alford 1999). Experimental work to disentangle such mechanisms would be of great interest, especially if cane toad larvae prove vulnerable to specific chemicals that do not affect the tadpoles of native frogs. Such work also could usefully explore the effects of environmental conditions on the degree to which toad larvae are affected by frog larvae; for example, waterbody attributes might influence the intensity or effects of such interactions (Warner, Travis & Dunson 1993; Mokany & Shine 2002).

Will these competitive effects also occur under field conditions? An extensive literature on other anuran species suggests that many of the same effects occur in natural waterbodies as in outdoor mesocosms and smaller experimental ponds (Alford 1999), but the intensity of competitive effects may differ considerably (Skelly 2002). The greatest obstacle to utilizing larval competition to reduce toad recruitment may be the prevalence of density-dependent effects. In many anurans, a reduction in larval density increases per-capita survival and growth rates (Alford 1999); and hence, even a major increase in mortality rates during larval life may have little impact on the number of metamorph toads recruiting from a waterbody. Field studies are needed to (1) quantify the degree to which reduced larval densities translate into reduced overall recruitment of metamorphs, (2) determine the effect of reduced recruitment on population biology and dispersal, and (3) compare the degree to which different frog species can affect toads in this respect. These studies will also need to assess the potential for interactive effects (Reylea 2004), because the impact of native frog tadpoles on recruitment of cane toad metamorphs may be affected by interspecific interactions in natural ponds with multi-species communities.

Density-dependent processes presumably operate at the metamorph stage of the life-history also, especially in the period soon after emergence when low desiccation tolerance forces the young toads to remain close to the water’s edge (Freeland & Kerin 1991; Cohen & Alford 1993; Child, Phillips & Shine 2008b; Child et al. 2008a). High metamorph densities at this time may result in competition for food or shelter-sites, and thus generate density-dependence in rates of growth and cumulative survival to juvenile size (Cohen & Alford 1993). The first month outside the water is a critical phase of the life-history, when mortality rates can be high and size-dependent (Cohen & Alford 1993). Importantly, much of that early mortality is due to factors that act most strongly against smaller-than-average metamorph toads. Size-dependence in vulnerability has been documented in response to predation (Ward-Fear et al. 2009), cannibalism (Pizzatto & Shine 2008), parasitism (Kelehear, Webb & Shine 2009) and desiccation (Child et al. 2008a). Thus, any competition-induced reduction in toad viability that results from larval interactions may persist into the terrestrial phase of the toad’s life-history, when density-dependent effects are weaker.

If native frogs can suppress toad recruitment, how have the invasive toads been able to spread so rapidly and successfully through Australia? As noted above, part of the answer may lie in habitat degradation and fungal infection, which have decimated frog populations in many areas (Tyler 1997; Jansen & Healey 2003). Thus, the expanding toad invasion front probably encountered many potential spawning sites virtually lacking in anuran competitors, especially since cane toads actively select highly disturbed waterbodies and surrounds for breeding (Hagman & Shine 2006; Semeniuk, Lemckert & Shine 2007). Although field-based tests of competitive suppression are needed, our results are broadly encouraging for a potential role of native frogs in reducing toad densities. If the frogs recruit to a degree that increases local population densities, competition for food between adult frogs and juvenile toads also might exacerbate the effects of larval competition. It should be straightforward logistically to increase densities of frog larvae in ponds, either by habitat manipulation (providing suitable calling-sites and spawning sites for adult frogs; Semeniuk, Lemckert & Shine 2007), or directly by adding tadpoles (either from captive breeding, or translocated from nearby waterbodies not used by toads). Obtaining such larvae is facilitated by the facts that many native frogs breed earlier than do cane toads, and the frog tadpoles generally have longer larval durations (Tyler 1994).

Artificially increasing frog-larval densities in toad-spawning sites would be of little value if most toad spawning sites already contained abundant frog larvae, but this is not the case. Instead, toad-spawning often is restricted to a minority of locally available ponds (Williamson 1999; Hagman & Shine 2006; Semeniuk, Lemckert & Shine 2007). Many native frogs utilize a broader range of spawning sites and thus, frogs commonly breed in large numbers in sites close to those used by toads (Williamson 1999; Hagman & Shine 2007). Although some of the sites used by breeding toads are in highly disturbed areas that lack native frogs, others are adjacent to frog-breeding sites. Such proximity would facilitate transfer of larvae among adjacent waterbodies (shorter transportation times will reduce costs, as well as the risk of adverse effects of transportation on frog tadpoles) and reduce potential problems such as disease transmission (i.e. source animals from more distant locations may be vectors of disease or parasites that are not present in the region of the release site). Lastly, frog tadpoles are likely to survive in most or all of the ponds used by toads, given extensive overlap in the physical and chemical (water-quality) attributes of ponds used by toads and those used by frogs (Hagman & Shine 2006; Semeniuk, Lemckert & Shine 2007), and frequent observations of toad-frog larval sympatry in the field (Crossland et al. 2008; Table 1). Given that toads dominate the tadpole community in many ephemeral anthropogenically disturbed ponds, collateral effects of introducing native frog tadpoles into such waterbodies are likely to be minor. In many cases, such introductions would be in areas where native frog populations have recently declined or become locally extinct due to human activities, and thus frog introductions could help to restore former populations. Nonetheless, the potential for collateral effects of introductions to natural ponds would need to be assessed prior to implementation; and in many highly disturbed sites, substantial restoration efforts would be needed if native frogs are to have any realistic hope of establishing viable populations.

Intensifying larval competition with native frogs will not provide a ‘silver bullet’ for control of invasive cane toads, but may be a valuable component of an integrated approach to toad control. Ideally, we would combine this potential weapon with other approaches, such as encouraging native predatory meat ants to forage at sites where metamorph cane toads are emerging (metamorph native frogs are at little risk from these predators, but toads are highly vulnerable: Ward-Fear et al. 2009), and encouraging native plants to grow along waterbody margins (thereby discouraging toad oviposition: Hagman & Shine 2006). All three of these approaches have a common theme: that we can manipulate native species to intensify their negative impacts on the invader. That approach entails less risk of untoward consequences than if other exotic organisms were introduced for biocontrol (the usual approach, Hays & Conant 2007) and is better-suited to uptake by the general public. Many people would be receptive to the idea of building up frog numbers to help combat toads, because native anurans are popular whereas cane toads are not (Woods 2000). Indeed, there are already books and websites devoted to encouraging the public to build frog-friendly ponds in their backyards (e.g. Casey 1996). The rationales for enhancing local frog populations include biocontrol of mosquitoes (Mokany & Shine 2002; Hagman & Shine 2007) and the idea of reducing toad recruitment could build on these existing motivations.

The strong effects produced by the green tree frog Litoria caerulea on cane toads in our study, as well as this species’ wide geographic distribution and high clutch sizes, make it an ideal candidate for attempts at biological control of cane toads in Australia. Also, rates of successful metamorphosis following exposure to cane toad tadpoles were higher for this species than for any other taxon that we tested. Importantly, this large and colourful species is already a popular pet (http://frogs.org.au/x/media/cs-caerulea.pdf), and hence encouragement to increase its numbers in the suburban habitats favoured by cane toads (Zug & Zug 1979) would be likely to attract enthusiastic community support.

In summary, our results suggest that it would be worth exploring the potential to increase densities of frog tadpoles in order to reduce viability of cane toad tadpoles. Clearly, many logistical obstacles still need to be overcome before any such method can be implemented at a broad scale. For example, we need further studies to evaluate the potential collateral impacts of increasing native frog abundances on other fauna, and to explore potential interactive effects of species additions in the complex assemblages of natural ponds. As well as the direct benefit to reducing ecological impact of the invasive toads, the habitat manipulations needed to encourage frog breeding and metamorph survival (notably, allowing dense vegetative growth near pond margins: Hagman & Shine 2006; Semeniuk, Lemckert & Shine 2007) would be beneficial to a wide variety of anuran species (including taxa whose conservation status is precarious) as well as other small vertebrate and invertebrate taxa (Langellotto & Denno 2004). Importantly, manipulations such as encouraging pond-side vegetation and translocating tadpoles are well-suited to local (e.g. school, community-group) abilities and enthusiasms. Such activities would contribute to public education about environmental issues and invasive-species threats, and may offer a low-risk approach with broad-ranging ecological benefits. Habitat restoration can confer major benefits for native species, even if competitive suppression of cane toad tadpoles by frog tadpoles is weak or non-existent; importantly, the potential ‘anti-toad’ benefits of encouraging native frogs may well be a powerful attractant for community-group involvement in such habitat-restoration activities.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank Greg Brown, Matt Greenlees and Lígia Pizzatto for assistance, and two anonymous reviewers for helpful criticisms of an earlier draft of this manuscript. The work was funded by the Australian Research Council, the National Council on Science and Technology of Mexico (CONACyT), the Australian Government, and the University of Sydney. Access to laboratory facilities was supported by the Northern Territory Land Corporation. Permits for the work were provided by the University of Sydney Animal Care and Ethics Committee, and the Parks and Wildlife Commission of the Northern Territory.

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  6. Discussion
  7. Acknowledgements
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